diff --git a/wp-includes/comment-functions.php b/wp-includes/comment-functions.php
index 1380422d4a..453b5a8107 100644
--- a/wp-includes/comment-functions.php
+++ b/wp-includes/comment-functions.php
@@ -2452,30 +2452,6 @@ function _prime_comment_caches( $comment_ids, $update_meta_cache = true ) {
 	}
 }
 
-/**
- * Lazy load comment meta when inside of a `WP_Query` loop.
- *
- * @since 4.4.0
- *
- * @param null $check      The `$check` param passed from the 'pre_comment_metadata' hook.
- * @param int  $comment_id ID of the comment whose metadata is being cached.
- * @return null In order not to short-circuit `get_metadata()`.
- */
-function wp_lazyload_comment_meta( $check, $comment_id ) {
-	global $wp_query;
-
-	if ( ! empty( $wp_query->comments ) ) {
-		// Don't use `wp_list_pluck()` to avoid by-reference manipulation.
-		$comment_ids = array();
-		foreach ( $wp_query->comments as $comment ) {
-			$comment_ids[] = $comment->comment_ID;
-		}
-		update_meta_cache( 'comment', $comment_ids );
-	}
-
-	return $check;
-}
-
 //
 // Internal
 //
diff --git a/wp-includes/comment-template.php b/wp-includes/comment-template.php
index 7b6e44c094..abb87f656b 100644
--- a/wp-includes/comment-template.php
+++ b/wp-includes/comment-template.php
@@ -1320,6 +1320,10 @@ function comments_template( $file = '/comments.php', $separate_comments = false
 	 * @param int   $post_ID  Post ID.
 	 */
 	$wp_query->comments = apply_filters( 'comments_array', $comments_flat, $post->ID );
+
+	// Set up lazy-loading for comment metadata.
+	add_action( 'get_comment_metadata', array( $wp_query, 'lazyload_comment_meta' ), 10, 2 );
+
 	$comments = &$wp_query->comments;
 	$wp_query->comment_count = count($wp_query->comments);
 	$wp_query->max_num_comment_pages = $comment_query->max_num_pages;
diff --git a/wp-includes/default-filters.php b/wp-includes/default-filters.php
index e3e2ad0c12..30974c2cae 100644
--- a/wp-includes/default-filters.php
+++ b/wp-includes/default-filters.php
@@ -200,7 +200,6 @@ add_filter( 'nav_menu_meta_box_object', '_wp_nav_menu_meta_box_object'        );
 add_filter( 'pingback_ping_source_uri', 'pingback_ping_source_uri'            );
 add_filter( 'xmlrpc_pingback_error',    'xmlrpc_pingback_error'               );
 add_filter( 'title_save_pre',           'trim'                                );
-add_filter( 'get_comment_metadata',     'wp_lazyload_comment_meta',     10, 2 );
 
 add_filter( 'http_request_host_is_external', 'allowed_http_request_hosts', 10, 2 );
 
diff --git a/wp-includes/query.php b/wp-includes/query.php
index 3ec605b513..f76c994ca1 100644
--- a/wp-includes/query.php
+++ b/wp-includes/query.php
@@ -1311,6 +1311,15 @@ class WP_Query {
 	 */
 	public $updated_term_meta_cache = false;
 
+	/**
+	 * Whether the comment meta cache for matched posts has been primed.
+	 *
+	 * @since 4.4.0
+	 * @access protected
+	 * @var bool
+	 */
+	public $updated_comment_meta_cache = false;
+
 	/**
 	 * Cached list of search stopwords.
 	 *
@@ -3682,6 +3691,11 @@ class WP_Query {
 			}
 		}
 
+		// If comments have been fetched as part of the query, make sure comment meta lazy-loading is set up.
+		if ( ! empty( $this->comments ) ) {
+			add_action( 'get_comment_metadata', array( $this, 'lazyload_comment_meta' ), 10, 2 );
+		}
+
 		if ( ! $q['suppress_filters'] ) {
 			/**
 			 * Filter the array of retrieved posts after they've been fetched and
@@ -4816,6 +4830,50 @@ class WP_Query {
 
 		return $check;
 	}
+
+	/**
+	 * Lazy-load comment meta when inside of a `WP_Query` loop.
+	 *
+	 * This method is public so that it can be used as a filter callback. As a rule, there is no need to invoke it
+	 * directly, from either inside or outside the `WP_Query` object.
+	 *
+	 * @since 4.4.0
+	 *
+	 * @param null $check      The `$check` param passed from the 'pre_comment_metadata' hook.
+	 * @param int  $comment_id ID of the comment whose metadata is being cached.
+	 * @return null In order not to short-circuit `get_metadata()`.
+	 */
+	public function lazyload_comment_meta( $check, $comment_id ) {
+		/*
+		 * We only do this once per `WP_Query` instance.
+		 * Can't use `remove_action()` because of non-unique object hashes.
+		 */
+		if ( $this->updated_comment_meta_cache ) {
+			return $check;
+		}
+
+		// Don't use `wp_list_pluck()` to avoid by-reference manipulation.
+		$comment_ids = array();
+		if ( is_array( $this->comments ) ) {
+			foreach ( $this->comments as $comment ) {
+				$comment_ids[] = $comment->comment_ID;
+			}
+		}
+
+		/*
+		 * Only update the metadata cache for comments belonging to these posts if the comment_id passed
+		 * to `get_comment_meta()` matches one of those comments. This prevents a single call to
+		 * `get_comment_meta()` from priming metadata for all `WP_Query` objects.
+		 */
+		if ( in_array( $comment_id, $comment_ids ) ) {
+			update_meta_cache( 'comment', $comment_ids );
+			$this->updated_comment_meta_cache = true;
+		} elseif ( empty( $comment_ids ) ) {
+			$this->updated_comment_meta_cache = true;
+		}
+
+		return $check;
+	}
 }
 
 /**
diff --git a/wp-includes/version.php b/wp-includes/version.php
index 9dfdbc2e6c..1998764a9d 100644
--- a/wp-includes/version.php
+++ b/wp-includes/version.php
@@ -4,7 +4,7 @@
  *
  * @global string $wp_version
  */
-$wp_version = '4.4-alpha-34710';
+$wp_version = '4.4-alpha-34711';
 
 /**
  * Holds the WordPress DB revision, increments when changes are made to the WordPress DB schema.